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J Am Soc Nephrol 14:493-499, 2003
© 2003 American Society of Nephrology

Donor Tissue Characteristics Influence Cadaver Kidney Transplant Function and Graft Survival but Not Rejection

Sita Gourishankar*, Gian S. Jhangri{dagger}, Sandra M. Cockfield* and Philip F. Halloran*

*Department of Medicine, Division of Nephrology and Immunology; and {dagger}Departments of Public Health Sciences, University of Alberta, Edmonton, Alberta, Canada.

Corrspondence to Dr. Philip F. Halloran, Director, Division of Nephrology and Immunology, University of Alberta, 250 Heritage Medical Research Centre, Edmonton, Alberta, Canada, T6G 2S2. Phone: 780-407-8880; Fax: 780-407-3417;


   Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
ABSTRACT. Acute injury and age are characteristics of transplanted tissue that influence many aspects of the course of a renal allograft. The influence of donor tissue characteristics on outcomes can be analyzed by studying pairing, the extent to which two kidneys retrieved from the same cadaver donor manifest similar outcomes. Pairing studies help to define the relative role of donor-related factors (among pairs) versus non-donor factors (within pairs). This study analyzed graft survival for 220 pairs of cadaveric kidneys for the similarity of parameters reflecting function and rejection. It also examined whether the performance of one kidney was predicted by the course of its "mate," the other kidney from that donor. Parameters reflecting function showed sustained pairing posttransplantation, as did graft survival. In contrast, measures of rejection strongly affected survival but showed no pairing. Surprisingly, the survival of a kidney was predicted by the early performance of its mate, an observation we term the "mate effect." Six-month graft survival and renal function were reduced in grafts for which the mate kidney displayed any criteria for functional impairment (dialysis dependency, low urine output [<=1 L] in the first 24 h posttransplant or day-7 serum creatinine >= 400 µmol/L), even for kidneys which themselves lacked those criteria. Rejection measures did not demonstrate the mate effect. In conclusion, kidney transplant function is strongly linked to donor-related factors (age, brain death). In contrast, rejection affects survival and function, but it is not primarily determined by the characteristics of the donor tissue. Graft survival reflects both of these influences. E-mail: phil.halloran@ualberta.ca


   Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
The shortage of cadaver donor kidneys causes transplant centers to accept more organs from marginal donors to serve the growing number of patients on the waiting list (1). The pressure to use organs from marginal donors underscores the importance of understanding the influence of donor tissue quality or characteristics on graft outcomes (2–4). Donor factors influence initial graft function and survival (5–8). In addition to donor age (9) and mode of brain death (10), other influential donor parameters include gender (11), whether the donor heart is beating (12), hypertension, and cardiovascular disease (13,14). The increased survival of kidney allografts from living donors compared with cadaver allografts with similar HLA mismatches is probably related, at least in part, to injury from brain death (15).

One approach to estimating the strength of donor factors is to compare outcomes of two kidneys from one donor, an approach akin to twin studies for identifying genetic versus environmental influences on disease phenotype (16). The two kidneys harvested from one donor constitute a pair and are the mate to one another. A comparison of inter-pair versus intra-pair variations should reflect the relative strength of donor factors compared with non-donor factors, which act later. The strength of pairing is that it is an indirect measure of "tissue quality" i.e., characteristics of the transplanted tissue affect its function and survival, including its ability to withstand stress and repair injuries. Cosio et al. (17) demonstrated that early function is paired for mate kidneys up to 6 mo. The two kidneys from the same donor share similar experiences up to the time of separation, including aging and donor diseases, brain death–related stress, and donor instability preceding vascular clamping.

In this study, we compared mate kidneys for the similarity of function (low urine output, dialysis dependency, serum creatinine [SCr]), as well as rejection and graft survival. We confined the study to our own center because we transplant both donor kidneys locally in almost all cases, thus avoiding the possible role of differences between centers. We also studied whether the performance of a kidney can be predicted by the early events in the mate kidney, an influence we call the "mate effect."


   Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Patient Characteristics
This study involved 440 adult cadaveric renal allograft recipients transplanted at the University of Alberta Hospital between February 1990 and March 2000. The study endpoint was December 31, 2000, which provided a range of follow-up of 10 mo to 10 yr. Recipients are subdivided into pairs, each receiving a kidney from the same donor. All donors met criteria for brain death (18). All kidneys were obtained with informed consent by the organ procurement organization, had a negative cytotoxic crossmatch at the time of transplantation, and were preserved in situ with University of Wisconsin solution. Implantation biopsies were routinely performed in over 95% of renal transplant recipients.

Posttransplant, all 440 subjects received the standard immunosuppressive regimen of a calcineurin inhibitor (approximately 80% of subjects received cyclosporine), prednisone, and either azathioprine (before 1995; 53.9%), or mycophenolate mofetil (MMF; 1995 and after; 46.1%); 38 subjects were on investigational drugs. As our immunosuppressive regimens were consistent and changed homogenously after 1995, recipients from the same donor received similar immunosuppressive drug (ISD) regimens in the majority of cases. Antilymphocyte globulin or OKT3 as induction therapy were not routinely used other than in recipients with poor early function or at high immunologic risk due to previous grafts or anti-HLA antibodies.

Definitions of Outcomes
End of follow-up for each patient was defined as either the date of death, graft failure, or the study endpoint. Diagnosis of acute transplant rejection (AR) was based on clinical criteria (sustained rise in SCr) and was confirmed in many cases (50%) by kidney biopsy. Rejection measures consisted of early rejection defined as any rejection episode within 6 mo of transplantation and severe rejection defined as any rejection requiring antibody therapy (OKT3 or anti-lymphocyte globulin). The three measures of early graft function analyzed were dialysis dependency in the first week, SCr >= 400 µmol/L at day 7, and low urine output, defined as in previous studies from this center (19) as less than 1 L of urine output in the first 24 h posttransplant. Induction therapy was also analyzed. Univariate analysis was performed using these six outcome variables for each pair; no multivariate analysis was performed. We did not analyze waiting time of recipients or PRA status. Allograft function, represented by SCr and calculated GFR, was examined at multiple times, from 6 mo to 8 yr posttransplant. Allograft survival was analyzed with patient death censored and as death with function included.

Statistical Analyses
Data are expressed as means ± SD. SCr values were normalized by logarithmic transformation. The relative impact of donor factors on SCr was investigated by an ANOVA of the SCr at several time points posttransplant. The relationship between SCr at several time points after transplantation was determined by Spearman rank correlation. We randomly assigned each kidney in a pair as #1 or #2 and used {chi}2 analysis to investigate the mate kidney relationships for graft survival, function, and rejection. Kaplan-Meier analysis was used to compare graft survival curves, and Cox proportional hazard regression was used to estimate the relative risk (RR) of different outcomes (low urine output, SCr >= 400 µmol/L, dialysis dependency at 1 wk, early and severe rejection) between pairs of recipients. GFR was calculated using the Cockcroft-Gault formula (20).


   Results
Top
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
The characteristics of the donor and recipient populations are summarized in Table 1. Results were similar for analyses done with and without death with function included. Therefore we will mainly discuss the results for analyses that censored death with function.


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  		Table 1. Characteristics of the recipient and donor population
 
Graft Survival
We analyzed whether the two kidneys from one donor had similar graft survival, censoring for death with a functioning graft. In 150 pairs, both kidneys survived; in 20 pairs, both kidneys failed; in 50 pairs, one graft failed but the other survived (P < 0.001). This indicates that graft failure showed a significant tendency to be paired.

Function and Rejection in Kidneys from the Same Donor
Comparing the differences among pairs to the differences within pairs allows us to assess the relative role of donor versus non-donor factors on various outcomes. We examined variability in function (SCr) as determined by donor and non-donor factors through an ANOVA (Table 2). The differences among pairs (donor factors) accounted for 54 to 77% of the variability in SCr, whereas intra-pair differences (non-donor factors) accounted for 23 to 46%. This relationship was sustained indefinitely, for as long as there were sufficient numbers to analyze.


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  		Table 2. Analysis of the variability and correlation in serum creatinine values in functioning kidneysa after cadaveric renal transplantation
 
We also examined the similarity of function in mate kidneys by performing a correlation analysis of SCr at various times posttransplant up to year 10 (Table 2). The SCr values for mate kidneys correlated significantly until the number of cases declined beyond 8 yr (n = 15). Beyond year 8, there was insufficient data to permit analysis. Calculated GFR showed similar correlation at month 6 (r = 0.29; P < 0.001; n = 156) and year 1 (r = 0.26; P < 0.002; n = 139), continuing to year 8.

We also assessed three measures of early renal function: dialysis dependency in the first week, low urine output in the first 24 h, and SCr >= 400 µmol/L by day 7. The latter two measures showed significant similarity in the kidneys derived from the same donor (Table 3). However, early dialysis dependency was not significantly paired. Moreover, early rejection and severe rejection did not show significant pairing (Table 3). Finally, induction therapy was not paired (data not shown).


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  		Table 3. Analysis of pairing of function and rejection outcomes
 
The Mate Effect
Early graft function reflects in part the characteristics of the donor tissue (6,21,22), and influences graft survival. The performance of the mate kidney thus provides additional information about donor tissue characteristics relevant to the kidney of interest. We studied whether adverse events (dysfunction or rejection) observed in the mate kidney altered the probability of graft survival in the kidney of interest. Kidneys of interest were divided into four groups (NN, NY, YN, YY) on the basis of whether they and/or the mate kidney met the criteria for the adverse event (Figure 1, A through C; Table 4). In each group, the first letter designates the presence (Y) or absence (N) of an adverse outcome in the kidney of interest; the second letter designates the presence or absence of the adverse event in the mate kidney.



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  		Figure 1. Kaplan-Meier plots of renal allograft survival in pairs of recipients: (A) dialysis dependency in first week posttransplant; (B) low urine output defined as <=1 L in first 24 h posttransplant; (C) serum creatinine >= 400 µmol/L at day 7; (D) acute rejection (AR) within first 6 mo; (E) AR requiring antibody (Ab) therapy.

 

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  		Table 4. The effect of adverse events in the mate kidney on death-censored and death-includeda graft survival of the kidney of interest
 
We assigned NN (i.e., neither kidney had the adverse event) a baseline RR for graft loss of 1.0. We compared the NN group to the NY group, in which the kidney of interest lacks the adverse event but its mate has the event. The relative risk of graft failure for the kidney of interest was calculated using Cox proportional hazard models for the four different groupings. We found that poor function (early dialysis dependency, low urine output, or SCr >= 400 µmol/L at day 7) in the mate kidney was significantly associated with failure of the kidney of interest, even when the kidney of interest does not have poor function (compare NN versus NY). However, graft loss in the kidney of interest was increased by early rejection or severe rejection in that kidney but not by rejection in the mate kidney (Figure 1, D and E; Table 4). Notably, no mate effect was seen for kidneys that failed due to technical failures or for nonfunctioning kidneys (data not shown).

We further examined whether the link between survival of a kidney and adverse function observed in its mate can be explained by the fact that mate performance reflects the shared stresses on donor organs before separation. The hypothesis is that kidneys for which mates showed early dysfunction would themselves function less well. This proved true for dialysis dependency and low urine output (Table 5); kidneys which themselves lacked these outcomes but for which the mate met these criteria displayed higher SCr values at day 7 and at 6 mo. Rejection was also more frequent in kidneys for which the mate required dialysis in the first week. However, SCr >= 400umol/L in the mate kidney was not associated with reduced function or increased rejection in the kidney of interest.


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  		Table 5. The function and rejection status of the kidney of interest compared by function status (SCr [µmol/L]) at day 7 and month 6 of the mate kidney
 

   Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
In this study, we examined the similarity in the course of two kidneys from one donor and the extent to which the survival of a kidney was predicted by the performance of the mate kidney. Performing this analysis within one center and one organ procurement organization is an advantage because it avoids the poorly understood "center effects" (23,24). This is facilitated by our program’s remote location, which mandates transplantation of both kidneys locally in almost all cases. We found that graft survival and SCr at all times posttransplant were similar in the kidneys from one donor. Moreover the survival of a kidney was strongly predicted by the early performance of its mate kidney as well as by its own early performance, an observation we term the mate effect. In contrast, the probability of rejection was not significantly paired in the kidneys from one donor, and rejection in the mate did not predict reduced survival of the kidney of interest. Whereas rejection is driven mainly by non-donor factors, graft function is driven by donor factors, some of which can be deduced from the performance of the mate kidney. These results indicate that the characteristics of the transplanted tissue have an enduring effect on graft function and survival, that the early events in the mate kidney can reveal important information about the donor tissue, and that donor tissue characteristics are not the major factor in the probability of rejection.

The similarity in function between the paired kidneys early and late shows that the effect of donor tissue characteristics is both powerful and sustained. Estimates of GFR are strongly associated with graft survival times (25); therefore, this is one mechanism by which donor factors influence outcomes (26). The donor determinants of GFR may include age (27,28) and the effect of brain death (21,27–30). Some donor effects could be attributed to increased rejection, but it is more likely to be mediated by the number of nephrons transplanted and surviving the transplant process. Rejection is not strongly paired; it is therefore unlikely that rejection explains pairing of function.

The function and survival of a kidney tends to be impaired when its mate meets criteria for poor function, compared with kidneys whose mate performs well. Furthermore, the mate effect on survival may be mediated by suboptimal function in kidneys that do not meet definitions of poor early function. We observed that kidneys that did not have dialysis in the first week or low urine output but for which mate did had higher SCr at 7 d and 6 mo. This is similar to the observation that cadaver kidneys that lack criteria for delayed graft function but have reduced function ("slow graft function") perform like kidneys with delayed graft function (31). Thus conventional definitions of poor early transplant function may be inadequate, and broader definitions of impaired function may be more appropriate (31).

The fact that neither dialysis dependency in the first week posttransplant nor rejection were strongly paired may reflect the greater influence of non-donor factors on these outcomes, such as cold ischemia time (32) and immunologic risks (presensitization and HLA mismatch) (33–35). In a small study, some pairing may be missed; therefore, the conclusion is not that donor factors have no role on dialysis dependency or rejection, but that the other factors are more important. We also acknowledge that these results may be altered in populations at higher risk, such as a primarily African-American population.

We and others (36) have previously postulated that tissue injury, by evoking inflammation, increases the probability of rejection and that injured kidneys are treated for rejection more frequently (20) than those with good immediate function. However, the present results argue against tissue injury being a strong determinant of rejection; specifically, the relative weakness of pairing of rejection suggests that donor tissue characteristics are not strong determinants of the probability of rejection. It is also probable that donor tissue influences on the posttransplant course are heterogeneous, with immediate and long-term components. Perhaps the level of function is more influenced by long-term influences on the tissue (nephron number, senescence, capacity for repair), whereas acute injury such as cold ischemia has more influence on inflammation and rejection.

The fact that the survival and function of a cadaver kidney correlates to some extent with the early performance of the mate kidney indicates the persisting legacy of the donor influences and may be useful clinically. The mate effect indicates that there are two sets of observations about donor tissue quality for a transplanted kidney: the performance of the kidney and the performance of its mate. For example, a kidney experiencing poor function in the face of excellent function in the mate raises the likelihood that the poor function is related to the recipient environment such as rejection or technical problems. Thus the performance of the mate should be part of the data available to a clinician to aid in interpreting the course of a kidney transplant. It may also be a factor in analyzing function in clinical trials that contain paired kidneys, because renal function is being considered as a potential end point for future clinical trials in transplantation.


   Acknowledgments
 
We thank Rob Huizinga, RN. We are also grateful for grant support from Canadian Institutes of Health Research, the Roche Organ Transplant Research Foundation, the Kidney Foundation of Canada, Novartis Pharmaceuticals Canada, Inc., The Muttart Foundation, and The Royal Canadian Legion.


   Footnotes
 
Sita Gourishankar and Gian S. Jhangri made equal contributions to this article.


   References
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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Received for publication April 12, 2002. Accepted for publication September 21, 2002.




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